Genetic and morphological approaches distinguish the three sibling species of the anisakis simplex species complex, with a species designation as anisakis berlandi n. sp. for A. simplex sp. C (Nematoda: Anisakidae)

Journal of Parasitology

Volumn 100, Issue 2, 2014, Pages 199-214

  Mattiucci, Simonetta ^a   Cipriani, Paolo ^a,b   Webb, Stephen C ^c   Paoletti, Michela ^a,b   Marcer, Federica ^d   Bellisario, Bruno ^b   Gibson, David I ^e   Nascetti, Giuseppe ^b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF TUSCIA   (Italy)

^c CAWTHRON INSTITUTE   (New Zealand)

^d UNIVERSITY OF PADOVA   (Italy)

^e DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA; HELMINTH DNA; RIBOSOMAL SPACER DNA;

ALLOZYME; BIOLOGICAL CHARACTERISTICS; DOLPHIN; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC MARKER; HOST RANGE; HYBRID; IDENTIFICATION METHOD; MITOCHONDRIAL DNA; MORPHOLOGY; NEMATODE; NOMENCLATURE; PARASITE; PARSIMONY ANALYSIS; PHYLOGENETICS; RANGE SIZE; SPECIES COMPLEX; SYMPATRY;

ALLOMETRY; ANISAKIS; ANISAKIS BERLANDI; ANISAKIS PEGREFFII; ANISAKIS SIMPLEX; ARTICLE; BODY HEIGHT; FEMALE; GENETIC DISTANCE; GENETIC IDENTIFICATION; GENETIC SIMILARITY; GENETIC VARIABILITY; HAPLOTYPE; INTRASPECIFIC VARIATION; MALE; MINKE WHALE; MITOCHONDRIAL GENE; MONOPHYLY; MORPHOLOGICAL TRAIT; NEW ZEALAND; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE IDENTIFICATION; PARSIMONY ANALYSIS; PHYLOGENETIC TREE; PHYLOGENY; PILOT WHALE; SEQUENCE ALIGNMENT; SIBLING; SISTER GROUP; STENELLA; SYMPATRY; ALLELE; ANATOMY AND HISTOLOGY; ANIMAL; ANISAKIASIS; ATLANTIC OCEAN; CHEMISTRY; CLASSIFICATION; GENETICS; ITALY; MEDITERRANEAN SEA; MOLECULAR GENETICS; NORWAY; PACIFIC OCEAN; PARASITOLOGY; PRINCIPAL COMPONENT ANALYSIS; VETERINARY;

ATLANTIC OCEAN; ATLANTIC OCEAN (NORTHEAST); MEDITERRANEAN SEA; NEW ZEALAND;

ALLELES; ANIMALS; ANISAKIASIS; ANISAKIS; ATLANTIC OCEAN; BASE SEQUENCE; DNA, HELMINTH; DNA, MITOCHONDRIAL; DNA, RIBOSOMAL SPACER; FEMALE; ITALY; MALE; MEDITERRANEAN SEA; MINKE WHALE; MOLECULAR SEQUENCE DATA; NEW ZEALAND; NORWAY; PACIFIC OCEAN; PHYLOGENY; PRINCIPAL COMPONENT ANALYSIS; SEQUENCE ALIGNMENT; STENELLA; WHALES, PILOT;

EID: 84911918027     PISSN: 00223395     EISSN: 19372345     Source Type: Journal    
DOI: 10.1645/12-120.1     Document Type: Article

References (54)

1. ABOLLO, E., C. GESTAL, AND S. PASCUAL. 2001. Anisakis infestation in marine fish and cephalopods from Galician waters: An updated perspective. Parasitology Research 87: 492-499.
2. BALDWIN, R. E., M. B. REW, M. L. JOHANSSON, M. A. BANKS, AND K. C. JACOBSON. JACOBSON. 2011. Population structure of three species of Anisakis nematodes recovered from Pacific sardines (Sardinops sagax) distributed throughout the California Current system. Journal of Parasitology 97: 545-554.
3. BERLAND, B. 1961. Nematodes from some Norwegian marine fishes. Sarsia 2: 1-50.
4. CAVALLERO, S., S. A. NADLER, L. PAGGI, N. B. BARROS, AND S. D'AMELIO. 2011. Molecular characterization and phylogeny of anisakid nematodes from cetaceans from south-eastern Atlantic coast of USA, Gulf of Mexico and Caribbean Sea. Parasitology Research 108: 781-792.
5. COBB, N. A. 1889. Beiträge zur Anatomie und Ontogenie der Nematoden. Jenaische Zeitschrift fü r Naturwissenschaft 23: 41-76.
6. D'AMELIO, S., K. D. MATHIOPOULOS, O. BRANDONISIO, G. LUCARELLI, F. DORONZO, AND L. PAGGI. 1999. Diagnosis of a case of gastric anisakidosis by PCR-based restriction fragment length polymorphism analysis. Parassitologia 41: 591-593.
7. DASCHNER, A., C. CUÉLLAR, AND M. RODERO. 2012. The Anisakis allergy debate: Does an evolutionary approach help? Trends in Parasitology 28: 9-15.
8. DAVEY, J. T. 1971. A revision of the genus Anisakis Dujardin, 1845 (Nematoda: Ascaridata). Journal of Helminthology 45: 51-72.
9. DE MEEÛS, T., K. D. MCCOY, PRUGNOLLE, F. C. CHEVILLON, P. DURAND, S. HURTREZ-BOUSSE, AND F. RENAUD. 2007. Population genetics and molecular epidemiology or how to 'dé busquer la bê te'. Infection, Genetics, and Evolution 7: 308-332.
10. FAGERHOLM, H. P. 1989. Intra-specific variability of the morphology in a single population of the seal parasite Contracaecum osculatum (Rudolphi) (Nematoda, Ascaridoidea), with a redescription of the species. Zoologica Scripta 18: 33-41.
11. FARRIS, J. S., M. KÄLLERSJÖ, A. G. KLUGE, AND C. BULT. 1994. Testing significance of incongruence. Cladistics 10: 315-319.
12. FELSENSTEIN, J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783-791.
13. FUMAROLA, L., R.MONNO, E. IERARDI, G. RIZZO, G. GIANNELLI, M. LALLE, AND E. POZIO. 2009. Anisakis pegreffii etiological agent of gastric infections in two Italian women. Foodborne Pathogen Diseases 6: 1157-1159.
14. GARBIN, L., S. MATTIUCCI, M. PAOLETTI, D. G. ACUÑA, AND G. NASCETTI. 2011. Genetic and morphological evidences for the existence of a new species of Contracaecum (Nematoda: Anisakidae) parasite Phalacrocorax brasilianis (Gmelin) from Chile and its genetic relationship with congeners from fish eating birds. Journal of Parasitology 97: 476-492.
15. HALL, T. A. 1999. BioEdit: A user-friendly biological sequence alignment and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98.
16. HILLIS, D. M., AND J. J. BULL. 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42: 182-192.
17. JOLLIFFE, I. T. 1986. Principal component analysis. Springer-Verlag, New York, 271 p.
18. JOMBART, T., S. DEVILLARD, AND F. BALLOUX. 2010. Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genetics 11: 94.
19. KIM, K. H., K. S. EOM, AND J. K. PARK. 2006. The complete mitochondrial genome of Anisakis simplex (Ascaridida: Nematoda) and phylogenetic implications. International Journal for Parasitology 36: 319-328.
20. LESSA, E. P. 1990. Multidimensional analysis of geographic genetic structure. Systematic Biology 39: 242-252.
21. MAYR, E. 1970. Populations, species and evolution: an abridgement of animal species and evolution. Harvard University Press, Cambridge, Massachusetts, 445 p.
22. MATTIUCCI, S., P. ABAUNZA, L. RAMADORI, AND G. NASCETTI. 2004. Genetic identification of Anisakis larvae in European hake from Atlantic and Mediterranean waters for stock recognition. Journal of Fish Biology 65: 495-510.
23. -, V. FARINA, N. CAMPBELL, K. MACKENZIE, P. RAMOS, P. ABAUNZA, AND G. NASCETTI. 2008. Anisakis spp. larvae (Nematoda: Anisakidae) from Atlantic horse mackerel: Their genetic identification and use as biological tags for host stock identification. Fisheries Research 89: 146-151.
24. -, P. FAZII, A. DE ROSA, M. PAOLETTI, A. SALOMONE MEGNA, A. GLIELMO, M.DE ANGELIS, A. COSTA, C. MEUCCI, V. CALVARUSO ET AL. 2013. Anisakiasis and gastroallergic reactions associated to Anisakis pegreffii infection, Italy. Emerging Infectious Diseases 19: 496-499.
25. -, AND G. NASCETTI. 2006. Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: An update. Parasite 13: 99-113.
26. -, AND -. 2008. Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host-parasite co-evolutionary processes. Advances in Parasitology 66: 47-148.
27. -, -, R. CIANCHI, L. PAGGI, P. ARDUINO, L. MARGOLIS, J. BRATTEY, S. C. WEBB, S. D'AMELIO, P.ORECCHIA ET AL. 1997. Genetic and ecological data on the Anisakis simplex Complex, with evidence for a new species (Nematoda, Ascaridoidea, Anisakidae). Journal of Parasitology 83: 401-416.
28. -, -, M. DAILEY, S. C. WEBB, N. BARROS, R. CIANCHI, AND L. BULLINI. 2005. Evidence for a new species of Anisakis Dujardin morphological description and genetic relationships between congeners (Nematoda: Anisakidae). Systematic Parasitology 61: 157-171.
29. -, L. PAGGI, G. NASCETTI, E. ABOLLO, S. C. WEBB, S. PASCUAL, R. CIANCHI, AND L. BULLINI. 2001. Genetic divergence and reproductive isolation between Anisakis brevispiculata and Anisakis physeteris (Nematoda: Anisakidae). International Journal for Parasitology 31: 9-14.
30. -, -, -, C. PORTES SANTOS, G.COSTA, A. P. DI BENEDITTO, R. RAMOS, M. ARGYROU, R. CIANCHI, AND L. BULLINI. 1997. Genetic markers in the study of Anisakis typica (Diesing, 1860): Larval identification and genetic relationships with other species of Anisakis Dujardin, 1845 (Nematoda: Anisakidae). Systematic Parasitology 51: 159-170.
31. -, M. PAOLETTI, F. BORRINI, M. PALUMBO, R. M. PALMIERI, V. GOMES, A. CASATI, AND G. NASCETTI. 2011. First molecular identification of the zoonotic parasite Anisakis pegreffii Nematoda: Anisakidae) in a paraffin-embedded granuloma taken from a case of human intestinal anisakiasis in Italy. BMC Infectious Diseases 11: 82.
32. -, -, A. CONSUEGRA SOLORZANO, AND G. NASCETTI. 2010. Contracaecum gibsoni n. sp. and C. overstreeti n. sp. (Nematoda: Anisakidae) from the Dalmatian pelican Pelecanus crispus (L.) in Greek waters: Morphological and genetic evidence. Systematic Parasitology 75: 207-224.
33. -, -, AND S. C. WEBB. 2009. Anisakis nascettii n. sp. (Nematoda: Anisakidae) from beaked whales of the southern hemisphere: Morphological description, genetic relationships between congeners and ecological data. Systematic Parasitology 74: 199-217.
34. -, -, -, N. SARDELLA, J. T. TIMI, B. BERLAND, AND G. NASCETTI. 2008. Genetic relationships among species of Contracaecum Railliet & Henry, 1912 and Phocascaris Höst, 1932 (Nematoda: Anisakidae) from pinnipeds based on mitochondrial cox2 sequences and congruence with allozyme data. Parasite 15: 408-419.
35. MOZGOVOY, A. A. 1953. [Ascaridata of animals and man and the diseases caused by them. Essentials of Nematodology 2.]. Akademiya Nauk SSSR, Moscow, Russia, 616 p. (In Russian.)
36. NADLER, S. A., S. D'AMELIO, M. D. DAILEY, L. PAGGI, S. SIU, AND J. A. SAKANARI. 2005. Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from Northern Pacific maritime mammals. Journal of Parasitology 91: 1413-1429.
37. -, AND D. S. S. HUDSPETH. 2000. Phylogeny of the Ascaridoidea (Nematoda: Ascaridida) based on three genes and morphology: Hypothesis of structural and sequence evolution. Journal of Parasitology 86: 380-393.
38. -, AND G. PÉREZ-PONCE DE LEÓN. 2011. Integrating molecular and morphological approaches for characterizing parasite cryptic species: Implications for parasitology. Parasitology 138: 1688-1709.
39. NASCETTI, G., L. PAGGI, P. ORECCHIA, J. W. SMITH, S. MATTIUCCI, AND L. BULLINI. 1986. Electrophoretic studies on the Anisakis simplex sp. complex (Ascaridida: Anisakidae) from the Mediterranean and North East Atlantic. International Journal for Parasitology 16: 633-640.
40. PAGGI, L., G. NASCETTI, S. WEBB, S. MATTIUCCI, R. CIANCHI, AND L. BULLINI. 1998. A new species of Anisakis Dujardin, 1845 (Nematoda, Anisakidae) from beaked whales (Ziphiidae): Allozyme and morphological evidence. Systematic Parasitology 40: 161-174.
41. PINA-MARTINS, F., AND O. S. PAULO. 2008. Concatenator: Sequence data matrices handling made easy. Molecular Ecology Resources 8: 1254-1255.
42. POSADA, D. 2008. jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 25: 1253-1256.
43. -, AND T. R. BUCKLEY. 2004. Model selection and model averaging in phylogenetics. Advantage of the AIC and Bayesian approaches over likelihood ratio test. Systematic Biology 53: 793-808.
44. QUIAZON, K. M. A., T. YOSHINAGA, K. OGAWA, AND R. YUKAMI. 2008. Morphological differences between larvae and in vitro-cultured adults of Anisakis simplex (sensu stricto) and Anisakis pegreffii (Nematoda: Anisakidae). Parasitology International 57: 483-489.
45. RICE, D. W. 1998. Marine mammals of the world: Systematics and distribution. Society for Marine Mammalogy, Special Publication Number 4, Lawrence, Kansas, 231 p.
46. R DEVELOPMENT CORE TEAM. 2012. R: A language and environment for the statistical computing. R. Foundation for Statistical Computing, Vienna, Austria.
47. REEDER, T.W. 2003. A phylogeny of the Australian Sphenomorphus group (Scincidae: Squamata) and the phylogenetic placement of the crocodile skins (Tribolonotus): Bayesian approaches to assessing congruence and obtaining confidence in maximum likelihood inferred relationships. Molecular Phylogenetics and Evolution 27: 384-397.
48. SHAMSI, S., R. GASSER, AND I. BEVERIDGE. 2012. Genetic characterization and taxonomy of species of Anisakis (Nematoda: Anisakidae) parasitic in Australian marine mammals. Invertebrate Systematics 26: 204-212.
49. SWOFFORD, D. L. 2003. PAUP*. Phylogenetic analysis using parsimony (*and other Methods). Sinauer Associates, Sunderland, Massachusetts.
50. -, R. B. SELANDER, AND W. C. BLACK. 1997. BIOSYS-2, a computer program for the analysis of allelic variation in population genetics and biochemical systematics. Colorado State University, Fort Collins, Colorado. Available at: ftp:// Iamar.edu/pub/wcb4. Accessed 1 December 2007.
51. TIMI, J. T., M. PAOLETTI, R. CIMMARUTA, A. N. LANFRANCHI, A. J. ALARCOS, L. GARBIN, M. GEORGE-NASCIMENTO, D. H. RODRÍGUEZ, G. V. GIARDINO, AND S. MATTIUCCI. 2013. Molecular identification, morphological characterization and new insights into the ecology of larval Pseudoterranova cattani in fishes from the Argentine coast with its differentiation from the Antarctic species, P. decipiens sp. E (Nematoda: Anisakidae). Veterinary Parasitology 199: 59-72.
52. UMEHARA, A., Y. KAWAKAMI, J. ARAKI, AND A. UCHIDA. 2007. Molecular identification of the etiological agent of the human anisakiasis in Japan. Parasitology International 56: 211-215.
53. VALENTINI, A., S. MATTIUCCI, P. BONDANELLI, S. C. WEBB, A. MIGNUCCIGIANNONE, M. M. COLOM-LLAVINA, AND G. NASCETTI. 2006. Genetic relationships among Anisakis species (Nematoda: Anisakidae) inferred from mitochondrial cox2 sequences and comparison with allozyme data. Journal of Parasitology 92: 156-166.
54. ZHU, X. Q., S. D'AMELIO, L. PAGGI, AND R. B. GASSER. 2000. Assessing sequence variation in the internal transcribed spacer of ribosomal DNA within and among members of the Contracaecum osculatum complex (Nematoda: Ascaridoidea: Anisakidae). Parasitology Research 86: 677-683.